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Many host-symbiont relationships are maintained through vertical transmission. While maternal symbiont transmission is common, biparental transmission is relatively rare. Protist-dependent termites are eusocial insects that harbor obligate, cellulolytic protists in their hindguts. Protists are vertically transmitted by winged reproductives (alates), which disperse to biparentally establish new colonies. Vertical transmission in protist-dependent termites is imperfect, as the protist communities of alates are often incomplete. Biparental transmission of protists may make it unnecessary for alates to harbor complete communities, as colonies would acquire symbionts from both founding kings and queens, which together may harbor sufficient inoculums. To investigate this hypothesis, the protist communities of Coptotermes gestroi and C. formosanus alates and colonies were examined using 18S rRNA amplicon sequencing. The complete protist communities of these Coptotermes species are composed of five parabasalid species each. Whereas alates often harbored 1–3 protist species, nearly all colonies harbored 4–5 species, implying biparental transmission. The probability of each protist species being present in at least one founding alate was used to determine expected protist occurrence in colonies. For most protists, expected and observed occurrence did not significantly differ, suggesting that each protist species only needs to be harbored by one founding alate to be acquired by colonies. Our results imply that biparental transmission allows founding reproductives to transmit adequate symbiont communities to colonies despite their individual communities being incomplete. We discuss biparental transmission in protist-dependent termites in the context of other biparentally transmitted symbioses.
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Protist symbionts of termites: diversity, distribution, and coevolution
ABSTRACT The symbiosis between termites and their hindgut protists is mutually obligate and vertically inherited. It was established by the late Jurassic in the cockroach ancestors of termites as they transitioned to wood feeding. Since then, protist symbionts have been transmitted from host generation to host generation by proctodeal trophallaxis (anal feeding). The protists belong to multiple lineages within the eukaryotic superphylum Metamonada. Most of these lineages have evolved large cells with complex morphology, unlike the non‐termite‐associated Metamonada. The species richness and taxonomic composition of symbiotic protist communities varies widely across termite lineages, especially within the deep‐branching clade Teletisoptera. In general, closely related termites tend to harbour closely related protists, and deep‐branching termites tend to harbour deep‐branching protists, reflecting their broad‐scale co‐diversification. A closer view, however, reveals a complex distribution of protist lineages across hosts. Some protist taxa are common, some are rare, some are widespread, and some are restricted to a single host family or genus. Some protist taxa can be found in only a few, distantly related, host species. Thus, the long history of co‐diversification in this symbiosis has been complicated by lineage‐specific loss of symbionts, transfer of symbionts from one host lineage to another, and by independent diversification of the symbionts relative to their hosts. This review aims to introduce the biology of this important symbiosis and serve as a gateway to the diversity and systematics literature for both termites and protists. A searchable database with all termite‐protist occurrence records and taxonomic references is provided as a supplementary file to encourage and facilitate new research in this field.
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- Award ID(s):
- 2045329
- PAR ID:
- 10481911
- Publisher / Repository:
- Wiley-Blackwell
- Date Published:
- Journal Name:
- Biological Reviews
- Volume:
- 99
- Issue:
- 2
- ISSN:
- 1464-7931
- Format(s):
- Medium: X Size: p. 622-652
- Size(s):
- p. 622-652
- Sponsoring Org:
- National Science Foundation
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